Epithelial Cell Polarity Alters Rho-GTPase Responses to Pseudomonas aeruginosa

Molecular Biology of the Cell

Volumn 15, Issue 2, 2004, Pages 411-419

  Kazmierczak, Barbara I ^a,c   Mostov, Keith ^a,b   Engel, Joanne N ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; MEMBRANE PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; BASOLATERAL MEMBRANE; CELL POLARITY; CELL STRAIN; CLOSTRIDIUM DIFFICILE; ENZYME ACTIVATION; ENZYME MECHANISM; EPITHELIUM CELL; HUMAN; HUMAN CELL; NONHUMAN; OPPORTUNISTIC INFECTION; POROSITY; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION;

ACTINS; ANIMALS; BACTERIAL TOXINS; CDC42 GTP-BINDING PROTEIN; CELL POLARITY; CELLS, CULTURED; CLOSTRIDIUM DIFFICILE; DOGS; EPITHELIAL CELLS; HELA CELLS; HUMANS; PSEUDOMONAS AERUGINOSA; RHO GTP-BINDING PROTEINS; RHOA GTP-BINDING PROTEIN; TIGHT JUNCTIONS;

ANIMALIA; BACTERIA (MICROORGANISMS); CLOSTRIDIUM; CLOSTRIDIUM DIFFICILE; NEGIBACTERIA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 0742288077     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E03-08-0559     Document Type: Article

References (49)

1. Anastasiadis, P.Z., Moon, S.Y., Thoreson, M.A., Mariner, D.J., Crawford, H.C., Zheng, Y., and Reynolds, A.B. (2000). Inhibition of RhoA by p120 catenin. Nat. Cell Biol. 2, 637-644.
2. Bacallao, R., Antony, C., Dotti, C., Karsenti, E., Stelzer, E.H.K., and Simons, K. (1989). The subcellular organization of Madin-Darby canine kidney cells during the formation of a polarized epithelium. J. Cell Biol. 109, 2817-2832.
3. Bagrodia, S., Taylor, S.J., Jordon, K.A., Van Aelst, L., and Cerione, R.A. (1998). A novel regulator of p21-activated kinases. J. Biol. Chem. 273, 23633-23636.
4. Benard, V., Bohl, B.P., and Bokoch, G.M. (1999). Characterization of Rac and Cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J. Biol. Chem. 274, 13198-13204.
5. Braga, V.M.M., Machesky, L.M., Hall, A., and Hotchin, N.A. (1997). The small GTPases Rho and Rac are required for the establishment of cadherin-dependent cell-cell contacts. J. Cell Biol. 137, 1421-1431.
6. Chen, L., Bagrodia, S., Cerione, R., and Galán, J. (1999). Requirement of p21-activated kinase (PAK) for Salmonella typhimurium-induced nuclear responses. J. Exp. Med. 189, 1479-1488.
7. Chen, L.-M., Hobbie, S., and Galan, J.E. (1996). Requirement of CDC42 for Salmonella-induced cytoskeletal and nuclear responses. Science 274, 2115-2118.
8. Cowell, B.A., Chen, D.Y., Frank, D.W., Vallis, A.J., and Fleiszig, S.M.J. (2000). ExoT of cytotoxic Pseudomonas aeruginosa prevents uptake by corneal epithelial cells. Infect. Immun. 68, 403-406.
9. Criss, A.K., Ahlgren, D.M., Jou, T.-S., McCormick, B.A., and Casanova, J.E. (2001). The GTPase Rac1 selectively regulates Salmonella invasion at the apical plasma membrane of polarized epithelial cells. J. Cell Sci. 114, 1331-1341.
10. de Bentzmann, S., Roger, P., Dupuit, F., Bajolet-Laudinat, O., Fuchey, C., Plotkowski, M.C., and Puchelle, E. (1996a). Asialo GM1 is a receptor for Pseudomonas aeruginosa adherence to regenerating respiratory epithelial cells. Infect. Immun. 64, 1582-1588.
11. de Bentzmann, S., Roger, P., and Puchelle, E. (1996b). Pseudomonas aeruginosa adherence to remodelling respiratory epithelium. Eur. Respir. J. 10, 2145-2150.
12. DiMango, E., Zar, H., Bryan, R., and Prince, A. (1995). Diverse Pseudomonas aeruginosa gene products stimulate respiratory epithelial cells to produce interleukin-8. J. Clin. Investig. 96, 2204-2210.
13. Evans, D.J., Kuo, T.C., Kwong, M., Van, R., and Fleiszig, S.M.J. (2002a). Mutation of csk, encoding the C-terminal Src kinase, reduces Pseudomonas aeruginosa internalization by mammalian cells and enhances bacterial cytotoxicity. Microb. Pathogen. 33, 135-143.
14. Evans, D.J., Maltseva, I.A., Wu, J., and Fleiszig, S.M.J. (2002b). Pseudomonas aeruginosa internalization by corneal epithelial cells involves MEK and ERK signal transduction proteins. FEMS Microbiol. Lett. 213, 73-79.
15. Fleiszig, S.M., Evans, D.J., Do, N., Vallas, V., Shin, S., and Mostov, K. (1997). Epithelial cell polarity affects susceptibility to Pseudomonas aeruginosa invasion and cytotoxicity. Infect. Immun. 65, 2861-2867.
16. Fleiszig, S.M., Vallas, V., Jun, C., Mok, L., Balkovetz, D., Roth, M., and Mostov, K. (1998). Susceptibility of epithelial cells to Pseudomonas aeruginosa invasion and cytotoxicity is upregulated by hepatocyte growth factor. Infect. Immun. 66, 3443-3446.
17. Fleiszig, S.M., Zaidi, T.S., and Pier, G.B. (1995). Pseudomonas aeruginosa invasion of and multiplication within corneal epithelial cells in vitro. Infect. Immun. 63, 4072-4077.
18. Frithz-Lindsten, E., Du, Y., Rosqvist, R., and Forsberg, A. (1997). Intracellular targeting of exoenzyme S of Pseudomonas aeruginosa via type III-dependent translocation induces phagocytosis resistance, cytotoxicity and disruption of actin microfilaments. Mol. Microbiol. 25, 1125-1139.
19. Garrett, W.S., Chen, L.-M., Kroschewski, R., Ebersold, M., Turley, S., Trombetta, S., Galan, J.E., and Mellman, I. (2000). Developmental control of endocytosis in dendritic cells by Cdc42. Cell 102, 325-334.
20. Garrity-Ryan, L., Kazmierczak, B., Kowal, R., Comolli, J., Hauser, A., and Engel, J. (2000). The arginine finger domain of ExoT is required for actin cytoskeleton disruption and inhibition of internalization of Pseudomonas aeruginosa by epithelial cells and macrophages. Infect. Immun. 68, 7100-7113.
21. Goehring, U.M., Schmidt, G., Pederson, K.J., Aktories, K., and Barbieri, J.T. (1999). The N-terminal domain of Pseudomonas aeruginosa exoenzyme S is a GTPase-activating protein for Rho GTPases. J. Biol. Chem. 274, 36369-36372.
22. Grassme, H., Jendrosser, V., Riehle, A., von Kurthy, G., Berger, J., Schwarz, H., Weller, M., Kolesnick, R., and Gulbins, E. (2003). Host defense against Pseudomonas aeruginosa requires ceramide-rich membrane rafts. Nat. Med. 9, 322-330.
23. Hauser, A.R., Kang, P.J., and Engel, J. (1998). PepA, a novel secreted protein of Pseudomonas aeruginosa, is necessary for cytotoxicity and virulence. Mol. Microbiol. 27, 807-818.
24. Hazlett, L.D., Masinick, S., Barrett, R., and Rosol, K. (1993). Evidence for asialo GM1 as a corneal glycolipid receptor for Pseudomonas aeruginosa adhesion. Infect. Immun. 61, 5164-5173.
25. Hobbie, S., Chen, L., Davis, R., and Galán, J. (1997). Involvement of mitogen-activated protein kinase pathways in the nuclear responses and cytokine production induced by Salmonella typhimurium in cultured intestinal epithelial cells. J. Immunol. 159, 5550-5559.
26. Hobert, M.E., Sands, K.A., Mrsny, R.J., and Madara, J.L. (2002). Cdc42 and Rac1 regulate late events in Salmonella typhimurium-induced interleukin-8 secretion from polarized epithelial cells. J. Biol. Chem. 277, 51025-51032.
27. Jou, T.-S., Schneeberger, E., and Nelson, W.J. (1998). Structural and functional regulation of tight junctions by RhoA and Rac1 small GTPases. J. Cell Biol. 142, 101-115.
28. Just, I., Selzer, J., Wilm, M., von Eichel-Streiber, C., Mann, M., and Aktories, K. (1995). Glucosylation of Rho proteins by Clostridium difficile toxin B. Nature 375, 500-503.
29. Kazmierczak, B., and Engel, J. (2002). Pseudomonas aeruginosa ExoT acts in vivo as a GTPase activating protein for RhoA, Rac1, and Cdc42. Infect. Immun. 70, 2198-2205.
30. Kazmierczak, B., Mostov, K., and Engel, J. (2001a). Interaction of bacterial pathogens with polarized epithelium. Annu. Rev. Microbiol. 55, 407-435.
31. Kazmierczak, B.I., Jou, T.-S., Mostov, K., and Engel, J. (2001b). Rho-GTPase activity modulates Pseudomonas aeruginosa internalization by epithelial cells. Cell Microbiol. 3, 85-98.
32. Krall, R., Schmidt, G., Aktories, K., and Barbieri, J.T. (2000). Pseudomonas aeruginosa ExoT is a Rho GTPase-activating protein. Infect. Immun. 68, 6066-6068.
33. Kroschewski, R., Hall, A., and Mellman, I. (1999). Cdc42 controls secretory and endocytic transport to the basolateral plasma membrane of MDCK cells. Nat. Cell Biol. 1, 8-13.
34. Lamaze, C., Fujimoto, L., Yin, H., and Schmid, S. (1997). The actin cytoskeleton is required for receptor-mediated endocytosis in mammalian cells. J. Biol. Chem. 272, 20332-20335.
35. Lee, A., Chow, D., Haus, B., Tseng, W., Evans, D., Fleiszig, S., Chandy, G., and Machen, T. (1999). Airway epithelial tight junctions and binding and cytotoxicity of Pseudomonas aeruginosa. Am. J. Physiol. 277, L204-L217.
36. Leung, S.M., Rojas, R., Maples, C., Flynn, C., Ruiz, W.G., Jou, T.S., and Apodaca, G. (1999). Modulation of endocytic traffic in polarized Madin-Darby canine kidney cells by the small GTPase rhoA. Mol. Biol. Cell 10, 4369-4384.
37. McCormick, B.A., Miller, S.I., Carnes, D., and Madara, J.L. (1995). Transepithelial signaling to neutrophils by salmonellae: a novel virulence mechanism for gastroenteritis. Infect. Immun. 63, 2302-2309.
38. Nobes, C.D., and Hall, A. (1999). Rho GTPases control polarity, protrusion and adhesion during cell movement. J. Cell Biol. 144, 1235-1244.
39. Noren, N.K., Liu, B.P., Burridge, K., and Kreft, B. (2000). p120 catenin regulates the actin cytoskeleton via Rho family GTPases. J. Cell Biol. 150, 567-579.
40. Pier, G.B., Grout, M., and Zaidi, T.S. (1997). Cystic fibrosis transmembrane conductance regulator is an epithelial cell receptor for clearance of Pseudomonas aeruginosa from the lung. Proc. Nat. Acad. Sci. USA 94, 12088-12093.
41. Plotkowski, M.C., de Bentzmann, S., Pereira, S.H., Zahm, J.M., Bajolet-Laudinat, O., Roger, P., and Puchelle, E. (1999). Pseudomonas aeruginosa internalization by human epithelial respiratory cells depends on cell differentiation, polarity, and junctional complex integrity. Am. J. Respir. Cell Mol. Biol. 20, 880-890.
42. Ren, X.-D., Kiosses, W.B., and Schwartz, M.A. (1999). Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 18, 578-585.
43. Roger, P., Puchelle, E., Bajolet-Laudinat, O., Tournier, J.M., Debordeaux, C., Plotkowski, M.C., Cohen, J.H., Sheppard, D., and de Bentzmann, S. (1999). Fibronectin and α5β1 integrin mediate binding of Pseudomonas aeruginosa to repairing airway epithelium. Eur. Respir. J. 13, 1301-1309.
44. Salyers, A.A., and Whitt, D.D. (eds.) (2002). Bacterial Pathogenesis: A Molecular Approach, Washington, DC: ASM Press.
45. Santos, M.F., McCormack, S.A., Guo, Z., Okolicany, J., Zheng, Y., Johnson, L.R., and Tigyi, G. (1997). Rho proteins play a critical role in cell migration during the early phase of mucosal restitution. J. Clin. Investig. 100, 216-225.
46. Tran Van Nhieu, G., and Sansonetti, P.J. (1999). Mechanism of Shigella entry into epithelial cells. Curr. Opin. Microbiol. 2, 51-55.
47. Tsang, K.W.T., Rutman, A., Tanaka, E., Lundt, V., Dewar, A., Cole, P.J., and Wilson, R. (1994). Interaction of Pseudomonas aeruginosa with human respiratory mucosa in vitro. Eur. Respir. J. 7, 1746-1753.
48. Yamaguchi, T., and Yamada, H. (1991). Role of mechanical injury on airway surface in the pathogenesis of Pseudomonas aeruginosa. Am. Rev. Respir. Dis. 144, 1147-1152.
49. Zahm, J.M., Chevillard, M., and Puchelle, E. (1991). Wound repair of human surface respiratory epithelium. Am. J. Respir. Cell Mol. Biol. 5, 242-248.